The Pith: The primary reason for the pervasiveness of sex among complex organisms is to maintain genomic integrity, not to increase genetic variation..

I just read a very strange article in the journal Evolution, Sex reduces genetic variation. In it the authors argue that contrary to conventional wisdom and evolutionary orthodoxy the rationale for the prevalence of sex amongst eukaryotic organisms is not maintenance of genetic variation, but rather a constraint upon genetic variation! This is a very peculiar view, and as someone not immersed in the literature on sex totally surprising to me.

The standard model is simple: sex allows organisms to swap genetic material and generate new combinations. This is at a particular premium for large, complex, and slow-breeding lineages, as is the norm amongst eukaryotes. In contrast, bacteria and their ilk have huge population sizes to draw from, and are quite literally protean in their ability to shift strategies to climb whatever adaptive landscape nature throws at them. Carl has a nice review of a paper in Science which reported just this finding in keeping with expectation. Increase the pathogen pressure, and eukaryotes which exchange genes marginalize those which do not because they can dodge the punches that their evolutionary adversaries throw in their direction.

The authors of the Evolution paper don’t deny that this is part of the story. Rather, they propose that this is a secondary part of the story. They acknowledge the power of microevolutionary pressure to modulate the basic genomic template on the margins where variation at the level of the gene is the target of selection. But, their contention is that by and large sexual reproduction’s primary value, which overrides the two-fold cost of sex, is to maintain the integrity of the genome of the parent. In other words, at the scale of the whole genome sex facilitates homogenization and stabilization of the basic ancestral template.

There seem two primary issues. Both of which I can not evaluate with any degree of confidence because of my lack of deep familiarity with the literature (no, I don’t check every single citation in a paper before reviewing it!). First, there’s the empirical issue, where the authors argue that in contrast to expectation asexual lineages are not more homogeneous or less diverse than sexual ones. The assumption has been contradicted, the authors assert, by new genomic techniques, though they grant that more work needs to be done. This very diversity and tendency to radiate in all directions argues against the stability of these asexual lineages. They also suggest that cancer, an asexual process, is a proper analogy for the riotous directional diversity of reproduction without sex (mitosis vs. meiosis in this case).

But perhaps more importantly within the paper there are some theoretical considerations. They argue that there is evidence that sex, as defined specifically by the process of meoisis and fusion of gametes, has a role to play in encouraging DNA repair, preventing the replication of chromosomal abnormalities, and dampening epigenetic variation. Let me quote their abstract:

…The common thread among many of these disciplines is that sex acts like a coarse filter, weeding out major changes, such as chromosomal rearrangements (that are almost always deleterious), but letting minor variation, such as changes at the nucleotide or gene level (that are often neutral), flow through the sexual sieve. Sex acts as a constraint on genomic and epigenetic variation, thereby limiting adaptive evolution. The diverse reasons for sex reducing genetic variation (especially at the genome level) and slowing down evolution may provide a sufficient benefit to offset the famed costs of sex.

Since the authors grant that sex does provide benefits in maintaining additive genetic variation at the level of the gene, it stands to reason that the mainstream research program should yield positive results. Rather, the thrust of this paper seems to be that this might be a case of looking for lost keys underneath the lamp-light. Ultimately I think this argument ties back into the unit of selection argument, though they seem to avoid that explosive issue in any explicit sense.

I’m somewhat a loss to really tote up the plausibility of this heterodox proposition with any clarity of conscience or confidence. Rather, I am curious as to what readers think? This did get published in Evolution, which from what I recall was created to midwife the Neo-Darwinian Synthesis. But I also know there are people who read this weblog who know quite a bit about DNA repair or epigenetics….

Well, in my experience, the people considering the orthodox ‘purpose of sex’ hypothesis are typically looking at the allele/locus scale, or the several allele/several locus scale; this seems to be focused on the genome scale. In a sense, it seems plausible, given the high rate of failure with initial reproduction steps (zygote inviability, etc). The ‘two-fold cost of sex’ is really swamped by huge inviability costs. Finding mates is only a problem is very sparse populations (and mathematics departments, where much of the original theory was generated).
In short, this is a very interesting hypothesis, which will require some careful thought to determine where the different costs and benefits predominate. The instincts of many undergraduates lead them to initially doubt the equivalence between bacterial sex and metazoan sex; it may very well be that the costs and benefits driving the different phenomena are indeed distinct, and that classic evolutionary biology has been confusing two categories in an attempt to make a hard problem tractable before the appropriate data were available.

dcwarrior

Is it that without some form of gene transfer and tying together of the genetic pool, there is no such thing as a species in the first place? And sex is one convenient way to make sure the population has a collective set of genes in common?

What would happen if there were no or much slower gene transfer? Then, each strain would take off in its own direction – would the term “species” mean as much then?

Considering that bacteria are still the most common form of life on earth, maybe sex isn’t necessarily an “advantage” in a head-to-head competition against bacteria, but it DOES make complex multicellular life possible? I.e., the advantages are at the macro level, while the disadvantages are at the micro level.

DK

I haven’t read the paper yet. From the abstract, it seems that they unnecessarily overemphasize the decrease in variation. The bottom line seems not controversial: there is a balance between reduction of genetic variation by filtering out one kind of mutations (large-scale chromosomal aberrations) and a boost of genetic variation by introduction of another kind of mutations (small scale). Without really looking into literature, I feel that there is pretty solid evidence that both the former and the latter can be beneficial.

John Roth

I think dcwarrior has the right end of the argument: the authors are contending that sex is what maintains the integrity of breeding populations (the replacement for the term “species.”) So the issue isn’t the integrity of any particular individual’s genome, it’s the integrity of the collective genome of the population.

Two other observations. First, the naive expectation that asexual reproduction, as in some species of lizards, would result in a population of identical clones, seems to ignore the amount of mutation that goes on independently of sex. It’s one of those things that appears obvious in retrospect.

Second, this might be a good foundation for discussions of group selection.

http://abugblog.blogspot.com Blackbird

I read it when it was online early and it made me think differently about the sex-asex debate. I think it is an important, illuminating paper and I’m glad you pick it up for review. This makes it easier to understand why many asexual species have mechanisms to maintain a functional genome such as gene conversion, polyploidy. Possibly sex is the best way evolution has come up with to keep a functional genome in the long term, and that might be the reason for the relative short life of asexual multicellular organisms.

Zwirko

Much of Metazoan evolution could be described as fiddling around with an ancient ancestral template with little in the way of innovation at the protein level (as compared to prokaryotes and viruses). I’m sure I’ve came across this hypothesis previously – can’t recall where or by whom though.

http://julianodea.blogspot.com/ Julian O’Dea

Also relevant is this recent paper by the late Professor Glansdorff and his colleagues:

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About Razib Khan

I have degrees in biology and biochemistry, a passion for genetics, history, and philosophy, and shrimp is my favorite food. In relation to nationality I'm a American Northwesterner, in politics I'm a reactionary, and as for religion I have none (I'm an atheist). If you want to know more, see the links at http://www.razib.com